Contrasting impacts of herbivore induction and elevated atmospheric CO₂ on silicon defences and consequences for subsequent herbivores

Abstract

Plants are often sequentially attacked by multiple herbivores; feeding by one herbivore can alter host plant quality that affects the performance of subsequent herbivores. Previous studies suggest that silicon (Si) is a highly inducible defence in grasses (Poaceae) following herbivory, so could mediate such temporally separated insect herbivore interactions. Elevated atmospheric CO2 concentrations (eCO2), in contrast, often reduce Si accumulation, which potentially weakens this interaction. We examined the effects of prior feeding by Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on the performance of crickets, Acheta domesticus (L.) (Orthoptera: Gryllidae), subsequently feeding on the same plant. We used Brachypodium distachyon (L.) P. Beauv. grass supplemented or non‐supplemented with Si and grown in the glasshouse maintained at ambient (aCO2) or eCO2 concentrations. As hypothesized, prior feeding by caterpillars induced Si accumulation. Despite eCO2 reducing Si accumulation, initial herbivore induction of Si negated the effects of eCO2. Both, previous caterpillar herbivory and Si supplementation reduced cricket performance. Si induction by successive herbivory was additive. Plant biomass was similar in plants attacked by caterpillars alone or both herbivores, suggesting that initial Si induction by caterpillars deterred feeding by crickets. Our results demonstrate that Si induction by one herbivore negatively impacts successive herbivores, as has been demonstrated for secondary metabolite‐mediated interactions. Uniquely, however, Si induction is an irreversible defence and potentially a stronger, or perhaps longer‐lasting mediator of such herbivore interactions in some plant taxa.

Bioactive Compounds, Functional Ingredients, Antioxidants, and Health Benefits of Edible Plants

“…The effects of CO 2 in this study on Si concentrations are broadly similar to the few studies exploring this, whereby elevated CO 2 leads to decreased Si accumulation (Ryalls et al, 2017;Biru et al, 2022;Johnson et al, 2022;Johnson et al, 2023), whereas reduced CO 2 leads to increased Si accumulation. To the best of our knowledge, the current study is only the third study to investigate the latter (Biru et al, 2020;Biru et al, 2021).…”

“…Understanding the diminishing levels of Si-based plant defences against herbivores under future elevated atmospheric CO 2 concentrations has received limited attention. Previous studies have shown that elevated CO 2 concentrations decrease Si accumulation in different Poaceae genera (e.g., grass species and wheat) Biru et al, 2022;Johnson et al, 2022), and this was associated with reduced Si defences while increasing herbivore performance; however, this effect is not always reproducible (Frew et al, 2017). The impact of elevated CO 2 on Si defences reflects that plants switch from Si defences to Cbased defences due to higher C availability under this scenario Johnson et al, 2022).…”

Silicon-mediated herbivore defence in a pasture grass under pre-industrial and Anthropocene levels of CO2

“…Moreover, Si is known to alter grass physical defences such as macrohairs, silica cells and prickle cells, which are linked to reduced feeding by insect herbivores (Hartley et al 2015, Biru et al 2021). Additionally, Si uptake and accumulation has been shown to be induced following herbivory (Massey et al 2007, Islam et al 2020, Biru et al 2022).…”

“…The lower production of frass under reduced CO 2 , which we used 2 concentrations decrease Si accumulation in different Poaceae genera (e.g. grasses species and wheat)(Johnson and Hartley 2018, Biru et al 2022, Johnson et al 2022, and this was associated with reduced Si defences while increasing herbivore performance; however, this effect is not always reproducible(Frew et al 2017). The impact of elevated CO 2 on Si defences re ect that plants switch from Si defences to C-based defences due to higher C availability Hartley 2018, Johnson et al 2022).…”

Variation in the Outcome of Plant-Mediated Pathogen Interactions in Potato: Effects of Initial Infections on Conspecific vs. Heterospecific Subsequent Infections

“…Plants are constantly under attack by above- and below-ground enemies such as viruses, bacteria, fungi, nematodes and insect herbivores (Stout et al 2006 ). The effects of these attackers can take place either simultaneously or sequentially, and in the latter case lead to plant-mediated indirect interactions where early-arriving attackers positively or negatively affect the performance of subsequent attackers (Wang et al 2014 ; Moreira et al 2015 ; Biru et al 2022 ). These plant‐mediated interactions are determined by the magnitude as well as type of plant responses which involve both mechanical (e.g.…”